Genetic architecture of cold tolerance in rice (Oryza sativa) determined through high resolution genome-wide analysis

Shakiba, Ehsan; Edwards, Jeremy D.; Jodari, F.; Duke, Sara E.; Baldo, Angela M.; Korniliev, Pavel; McCouch, Susan R.; Eizenga, G. C.

doi:10.1371/journal.pone.0172133

Cited by 124 publications

(124 citation statements)

References 75 publications

(109 reference statements)

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“…Wang et al (2016) identified 67 QTLs for cold tolerance at the seedling stage, and 56 of these QTLs were located in regions that had not been reported to contain cold tolerance-related QTLs. Shakiba et al (2017) identified 42 QTLs associated with cold tolerance at the seedling stage, 20 of which did not co-localize with previously reported cold-tolerant QTLs. Consequently, GWAS can identify new QTLs for cold tolerance and provide new insights into the genetic basis of cold tolerance in rice.…”

Section: Introductionmentioning

confidence: 57%

“…Most of these QTLs have been detected repeatedly using different bi-parental populations. Generally, japonica cultivars are more coldtolerant than indica cultivars (Shakiba et al 2017). Most bi-parental populations used in QTL analyses have been derived from a cross between a cold-tolerant japonica variety and a cold-sensitive indica variety; consequently, most QTLs associated with cold tolerance are derived from the japonica parent (Andaya and Mackill 2003;Kuroki et al 2007;Ma et al 2015;Zhu et al 2015).…”

Section: Introductionmentioning

confidence: 99%

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Genome-wide association study of cold tolerance of Chinese indica rice varieties at the bud burst stage

Zhang

et al. 2018

Plant Cell Rep

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Key message A region containing three genes on chromosome 1 of indica rice was associated with cold tolerance at the bud burst stage; these results may be useful for breeding cold-tolerant lines. Abstract Low temperature at the bud burst stage is one of the major abiotic stresses limiting rice growth, especially in regions where rice seeds are sown directly. In this study, we investigated cold tolerance of rice at the bud burst stage and conducted a genome-wide association study (GWAS) based on the 5K rice array of 249 indica rice varieties widely distributed in China. We improved the method to assess cold tolerance at the bud burst stage in indica rice, and used severity of damage (SD) and seed survival rate (SR) as the cold-tolerant indices. Population structure analysis demonstrated that the Chinese indica panel was divided into three subgroups. In total, 47 significant single-nucleotide polymorphism (SNP) loci associated with SD and SR, were detected by association mapping based on mixed linear model. Because some loci overlapped between SD and SR, the loci contained 13 genome intervals and most of them have been reported previously. A major QTL for cold tolerance on chromosome 1 at the position of 31.6 Mb, explaining 13.2% of phenotypic variation, was selected for further analysis. Through LD decay, GO enrichment, RNA-seq data, and gene expression pattern analyses, we identified three genes (LOC_Os01g55510, LOC_Os01g55350 and LOC_Os01g55560) that were differentially expressed between cold-tolerant and cold-sensitive varieties, suggesting they may be candidate genes for cold tolerance. Together, our results provide a new method to assess cold tolerance in indica rice, and establish the foundation for isolating genes related to cold tolerance that could be used in rice breeding.

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Section: Introductionmentioning

confidence: 57%

Section: Introductionmentioning

confidence: 99%

Genome-wide association study of cold tolerance of Chinese indica rice varieties at the bud burst stage

Zhang

et al. 2018

Plant Cell Rep

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“…At the germination stage, GWAS mapping of a collection of 63 rice varieties from Hokkaido, Japan identified 17 QTL (Fujino et al, 2015) and evaluation of the Rice Diversity Panel 1 (RDP1) revealed a total of 42 QTL (Shakiba et al, 2017). RDP1 seedlings at the three-leaf stage, were subjected to 3 days of chilling treatment, scored for chilling survivability and GWAS mapping revealed 67 QTL located on 11 chromosomes (Wang et al, 2016a).…”

Section: Introductionmentioning

confidence: 99%

Assessment of Five Chilling Tolerance Traits and GWAS Mapping in Rice Using the USDA Mini-Core Collection

et al. 2017

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Rice (Oryza sativa L.) is often exposed to cool temperatures during spring planting in temperate climates. A better understanding of genetic pathways regulating chilling tolerance will enable breeders to develop varieties with improved tolerance during germination and young seedling stages. To dissect chilling tolerance, five assays were developed; one assay for the germination stage, one assay for the germination and seedling stage, and three for the seedling stage. Based on these assays, five chilling tolerance indices were calculated and assessed using 202 O. sativa accessions from the Rice Mini-Core (RMC) collection. Significant differences between RMC accessions made the five indices suitable for genome-wide association study (GWAS) based quantitative trait loci (QTL) mapping. For young seedling stage indices, japonica and indica subspecies clustered into chilling tolerant and chilling sensitive accessions, respectively, while both subspecies had similar low temperature germinability distributions. Indica subspecies were shown to have chilling acclimation potential. GWAS mapping uncovered 48 QTL at 39 chromosome regions distributed across all 12 rice chromosomes. Interestingly, there was no overlap between the germination and seedling stage QTL. Also, 18 QTL and 32 QTL were in regions discovered in previously reported bi-parental and GWAS based QTL mapping studies, respectively. Two novel low temperature seedling survivability (LTSS)–QTL, qLTSS3-4 and qLTSS4-1, were not in a previously reported QTL region. QTL with strong effect alleles identified in this study will be useful for marker assisted breeding efforts to improve chilling tolerance in rice cultivars and enhance gene discovery for chilling tolerance.

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“…The challenge of global warming means that crop plants, including rice, will be more exposed to extreme growing environments, e.g., low and high temperatures. Although the response by rice to cold stress has been described (Zhi-guo et al, 2014; Wang D. et al, 2016; Shakiba et al, 2017), we still need to identify more effective genes that can regulate this response.…”

Section: Introductionmentioning

confidence: 99%

Genome-Wide Identification and Analysis of Genes, Conserved between japonica and indica Rice Cultivars, that Respond to Low-Temperature Stress at the Vegetative Growth Stage

et al. 2017

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Cold stress is very detrimental to crop production. However, only a few genes in rice have been identified with known functions related to cold tolerance. To meet this agronomic challenge more effectively, researchers must take global approaches to select useful candidate genes and find the major regulatory factors. We used five Gene expression omnibus series data series of Affymetrix array data, produced with cold stress-treated samples from the NCBI Gene Expression Omnibus (http://www.ncbi.nlm.nih.gov/geo/), and identified 502 cold-inducible genes common to both japonica and indica rice cultivars. From them, we confirmed that the expression of two randomly chosen genes was increased by cold stress in planta. In addition, overexpression of OsWRKY71 enhanced cold tolerance in ‘Dongjin,’ the tested japonica cultivar. Comparisons between japonica and indica rice, based on calculations of plant survival rates and chlorophyll fluorescence, confirmed that the japonica rice was more cold-tolerant. Gene Ontology enrichment analysis indicate that the ‘L-phenylalanine catabolic process,’ within the Biological Process category, was the most highly overrepresented under cold-stress conditions, implying its significance in that response in rice. MapMan analysis classified ‘Major Metabolic’ processes and ‘Regulatory Gene Modules’ as two other major determinants of the cold-stress response and suggested several key cis-regulatory elements. Based on these results, we proposed a model that includes a pathway for cold stress-responsive signaling. Results from our functional analysis of the main signal transduction and transcription regulation factors identified in that pathway will provide insight into novel regulatory metabolism(s), as well as a foundation by which we can develop crop plants with enhanced cold tolerance.

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Genetic architecture of cold tolerance in rice (Oryza sativa) determined through high resolution genome-wide analysis

Cited by 124 publications

References 75 publications

Genome-wide association study of cold tolerance of Chinese indica rice varieties at the bud burst stage

Genome-wide association study of cold tolerance of Chinese indica rice varieties at the bud burst stage

Assessment of Five Chilling Tolerance Traits and GWAS Mapping in Rice Using the USDA Mini-Core Collection

Genome-Wide Identification and Analysis of Genes, Conserved between japonica and indica Rice Cultivars, that Respond to Low-Temperature Stress at the Vegetative Growth Stage

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